Abstract
Host movement and spatial structure can strongly influence the ecology and evolution of infectious diseases, with limited host movement potentially leading to high spatial heterogeneity in infection. Monarch butterflies (Danaus plexippus) are best known for undertaking a spectacular long-distance migration in eastern North America; however, they also form non-migratory populations that breed year-round in milder climates such as Hawaii and other tropical locations. Prior work showed an inverse relationship between monarch migratory propensity and the prevalence of the protozoan parasite, Ophryocystis elektroscirrha. Here, we sampled monarchs from replicate sites within each of four Hawaiian Islands to ask whether these populations show consistently high prevalence of the protozoan parasite as seen for monarchs from several other non-migratory populations. Counter to our predictions, we observed striking spatial heterogeneity in parasite prevalence, with infection rates per site ranging from 4–85%. We next used microsatellite markers to ask whether the observed variation in infection might be explained by limited host movement and spatial sub-structuring among sites. Our results showed that monarchs across the Hawaiian Islands form one admixed population, supporting high gene flow among sites. Moreover, measures of individual-level genetic diversity did not predict host infection status, as might be expected if more inbred hosts harbored higher parasite loads. These results suggest that other factors such as landscape-level environmental variation or colonization-extinction processes might instead cause the extreme heterogeneity in monarch butterfly infection observed here.
Highlights
Much work during the past two decades has focused on understanding the spatial ecology of host-pathogen interactions
Movement can further result in gene flow and the spread of host resistance alleles across a landscape, with studies of anther-smut in plants and viruses in moths showing that limited host movement or gene flow can generate high spatial heterogeneity in prevalence, allowing some patches to become heavily infected while others remain disease-free [14,15,16]
Parasite prevalence was highly variable among and within the Hawaiian Islands. These results are unexpected, because the nonmigratory status of monarchs of the Hawaiian Islands would lead us to predict that parasite prevalence should be relatively high across all sites
Summary
Much work during the past two decades has focused on understanding the spatial ecology of host-pathogen interactions. Some studies have shown that genetic variation in traits affecting host resistance and pathogen virulence can generate spatial variation in infection patterns [1]. Other work demonstrated that landscape-level heterogeneity in factors such as habitat quality, the relative abundance of host species, and geographic features such as rivers and mountains, can affect the spatial spread and prevalence of pathogens [2,3,4]. Movement can further result in gene flow and the spread of host resistance alleles across a landscape, with studies of anther-smut in plants and viruses in moths showing that limited host movement or gene flow can generate high spatial heterogeneity in prevalence, allowing some patches to become heavily infected while others remain disease-free [14,15,16]
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